Abstract
The aim of this work was to evaluate the effect of consumption of extruded maize product added with a low level of the red seaweed Pyropia columbina on colonic and systemic oxidative status using a growing Wistar rat model. Twenty-four (n = 24) male Wistar rats were fed for 60 days with control (C), extruded maize product group (M), or extruded maize product added with red seaweed P. columbina (MP) diets. Rats fed whit MP showed higher catalase (CAT) and glutathione reductase (GR) colon expression than those fed with M or C. Beneficial effects on intestinal mucosal barrier function were observed, which was manifested in decrease of cecal pH (10%) and mucinase activity (67%) and increase of sIgA content (53%). Rats fed with MP diet showed lower cyclooxygenase-2 (COX-2; 43%), inducible nitric oxide synthase (iNOS; 49%), and NF-κβ transcription factor (27%) expression in distal colon than those fed with M or C diets. Also, MP diet exerted a significant antioxidant effect on the serum and liver, increasing hepatic redox index, CAT, and GR activity. Apparent calcium absorption, total skeleton bone mineral content, and bone mineral density of total body were the same among groups. The type of dietary fiber and phenolic compounds from P. columbina could promote antioxidant environment in growing Wistar rats.
Similar content being viewed by others
References
Albarracín M, Weisstaub A, Zuleta A, Mandalunis P, González R, Drago S (2014) Effects of extruded whole maize, polydextrose and cellulose as sources of fibre on calcium bioavailability and metabolic parameters of growing Wistar rats. Food Funct 5:804–810
Albarracín M, Weisstaub A, Zuleta A, Drago S (2016a) Extruded whole grain diets based on brown, soaked and germinated rice. Effects on the lipid profile and antioxidant status of growing Wistar rats. Part II. Food Funct 7:2729–2735
Albarracín M, Weisstaub A, Zuleta A, Drago S (2016b) Extruded whole grain diets based on brown, soaked and germinated rice. Effects on cecum health, calcium absorption and bone parameters of growing Wistar rats. Part I. Food Funct 7:2722–2728
AOAC (1995) Official methods of analysis of AOAC International, 16th edn. Horowitz, Washigton DC
Barnes P, Karin M (1997) Nuclear factor-κβ—a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 336:1066–1071
Cian R, López-Posadas R, Drago S, Sánchez de Medina F, Martínez-Augustín O (2012) Immunomodulatory properties of the protein fraction from Phorphyra columbina. J Agric Food Chem 60:8146–8154
Cian R, Caballero M, Sabbag N, Gonzalez R, Drago S (2014a) Bio-accessibility of bioactive compounds (ACE inhibitors and antioxidants) from extruded maize products added with a red seaweed Porphyra columbina. LWT-Food Sci Technol 55:51–58
Cian R, Fajardo M, Alaiz M, Vioque J, González R, Drago S (2014b) Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int J Food Sci Nutr 65:299–305
Cian R, Salgado P, Drago S, González R, Mauri A (2014c) Development of naturally activated edible films with antioxidant properties prepared from red seaweed Porphyra columbina biopolymers. Food Chem 146:6–14
Cian R, Drago S, Sánchez de Medina F, Martínez-Augustin O (2015) Proteins and carbohydrates from red seaweeds: evidence for beneficial effects on gut function and microbiota. Mar Drugs 13:5358–5383
Devasena T, Menon V (2003) Fenugreek affects the activity of β-glucuronidase and mucinase in the colon. Phytother Res 17:1088–1091
Dvir I, Chayoth R, Sod-Moriah U, Shany S, Nyska A, Stark A, Madar Z, Arad S (2000) Soluble polysaccharide and biomass of red microalga Porphyridium sp. alter intestinal morphology and reduce serum cholesterol in rats. Br J Nutr 84:469–476
Figueiredo F, Encarnação T, Campos M (2016) Algae as functional foods for the elderly. Food Nutr Sci 7:1122–1148
Fitzgerald C, Gallagher E, Tasdemir D, Hayes M (2011) Heart health peptides from macroalgae and their potential use in functional foods. J Agric Food Chem 59:6829–6836
Gavrieli Y, Sherman Y, Ben-Sasso S (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501
Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P (2012) Effect of the red seaweed Mastocarpus stellatus intake on lipid metabolism and antioxidant status in healthy Wistar rats. Food Chem 135:806–811
Goñi I, Jiménez-Escrig A, Gudiel M, Saura-Calixto F (2005) Artichoke (Cynara scolymus L) modifies bacterial enzymatic activities and antioxidant status in rat cecum. Nutr Res 25:607–615
Gressler V, Yokoya N, Fujii M, Colepicolo P, Mancini J, Torres R, Pinto E (2010) Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chem 120:585–590
Gudiel-Urbano M, Goñi I (2002) Effect of edible seaweeds (Undaria pinnatifida and Porphyra ternera) on the metabolic activities of intestinal microflora in rats. Nutr Res 22:323–331
Hamed I, Özogul F, Özogul Y, Regenstein J (2015) Marine bioactive compounds and their health benefits: a review. Compr Rev Food Sci 14:446–465
Holdt S, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597
Honkanen P (2009) Consumer acceptance of (marine) functional food. In: Luten J (ed) The Nordic Network on Marine Functional Food (MARIFUNC). Wageningen Academic Publishers, Oslo, pp 141–154
Isaka S, Cho K, Nakazono S, Abu R, Ueno M, Kim D, Oda T (2015) Antioxidant and anti-inflammatory activities of porphyran isolated from discolored nori (Porphyra yezoensis). Int J Biol Macromol 74:68–75
Iwai K (2008) Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-Ay mice. Plant Foods Hum Nutr 63:163–169
Jackson C, Dini J, Lavandier C, Rupasinghe H, Faulkner H, Poysa V, Buzzell D, De Grandis S (2002) Effects of processing on the content and composition of isoflavones during manufacturing of soy beverage and tofu. Process Biochem 37:1117–1123
Jiang Z, Hama Y, Yamaguchi K, Oda T (2012) Inhibitory effect of sulphated polysaccharide porphyran on nitric oxide production in lipopolysaccharide-stimulated RAW264.7 macrophages. J Biochem 151:65–74
Jiménez-Escrig A, Gómez-Ordóñez E, Rupérez P (2012) Brown and red seaweeds as potential sources of antioxidant nutraceuticals. J Appl Phycol 24:1123–1132
Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio M, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512
Katayama M, Fukuda T, Okamura T, Suzuki E, Tamura K, Shimizu Y, Suda Y, Suzuki K (2011) Effect of dietary addition of seaweed and licorice on the immune performance of pigs. Anim Sci J 82:274–281
Kim M, Kim J, Choi W, Lee S (2008) Effects of seaweed supplementation on blood glucose concentration, lipid profile, and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Nutr Res Pract 2:62–67
Königsberg Fainstein M (2007) Nrf2: La historia de un nuevo factor de transcripción que responde a estrés oxidativo. Revista de Educación Bioquímica 26:18–25
Kulshreshtha G, Rathgeber B, Stratton G, Thomas N, Evans F, Critchley A, Hafting J, Prithiviraj B (2014) Feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poult Sci 93:2991–3001
Kumar S, Brown L (2013) Seaweeds as potential therapeutic interventions for the metabolic syndrome. Rev Endocr Metab Disord 14:299–308
López-Oliva M, Pozuelo M, Rotger R, Muñoz-Martínez E, Goñi I (2013) Grape antioxidant dietary fibre prevents mitochondrial apoptotic pathways by enhancing Bcl-2 and Bcl-x L expression and minimising oxidative stress in rat distal colonic mucosa. Br J Nutr 109:4–16
Lowry O, Rosebrough N, Farr A, Randall R (1951) Proteins measurement with the folin phenol reagent. J Biol Chem 193:265–275
Macfarlane S, Macfarlane G, Cummings J (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24:701–714
Maynard L (1994) The Atwater system of calculating the caloric value of diets. J Nutr 28:443–452
Perez-Recalde M, Matulewicz M, Pujol C, Carlucci M (2014) In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from red seaweed Nemalion helminthoides. Int J Biol Macromol 63:38–42
Reeves P, Nielsen F, Fahey G (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951
Shiau S, Chang G (1983) Effects of dietary fiber on fecal mucinase and beta-glucuronidase activity in rats. J Nutr 113:138–144
Somogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23
Tsuge K, Okabe M, Yoshimura T, Sumi T, Tachibana H, Yamada K (2004) Dietary effects of porphyran from Porphyra yezoensis on growth and lipid metabolism of Sprague-Dawley rats. Food Sci Technol Res 10:147–151
Villanueva M, Morcillo M, Tenorio M, Mateos-Aparicio I, Andrés V, Redondo-Cuenca A (2014) Health-promoting effects in the gut and influence on lipid metabolism of Himanthalia elongata and Gigartina pistillata in hypercholesterolaemic Wistar rats. Eur Food Res Technol 238:409–416
Acknowledgements
All authors read and approved the final manuscript. The authors are thankful to CAI + D 2011 PI 0292 LI of the Universidad Nacional del Litoral for the financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cian, R.E., Llopart, E., López-Oliva Muñoz, M.E. et al. Low level of red seaweed Pyropia columbina added to extruded maize products promotes colonic and systemic antioxidant environment in growing Wistar rats. J Appl Phycol 30, 637–648 (2018). https://doi.org/10.1007/s10811-017-1259-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-017-1259-3